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Abstract

Chloroplast biogenesis is a fundamental process occurring during seedling ontogenesis and leading to plant autotrophy. Which membrane components sterically organize the light-triggered transition of etioplast prolamellar bodies (PLBs) into chloroplast thylakoids, and thus mediate cubic–}lamellar transformation, is poorly understood. Here, we used combined two- and three-dimensional electron microscopy, spectroscopy, and biochemical methods to determine the role of CURT1 proteins in the formation of etioplast cubic membranes and their transformation to photosynthetically active chloroplast thylakoids. CURT1 proteins were previously recognized as significant contributors to thylakoid membrane folding. We found that CURT1 proteins are integral proteins of etioplast membranes and act as factors modulating PLBs and prothylakoid nanomorphology. They are also required for concerted thylakoid maturation under de-etiolation.The term {“}de-etiolation{”} refers to the light-dependent differentiation of etioplasts to chloroplasts in angiosperms. The underlying process involves reorganization of prolamellar bodies (PLBs) and prothylakoids into thylakoids, with concurrent changes in protein, lipid, and pigment composition, which together lead to the assembly of active photosynthetic complexes. Despite the highly conserved structure of PLBs among land plants, the processes that mediate PLB maintenance and their disassembly during de-etiolation are poorly understood. Among chloroplast thylakoid membrane{–localized proteins, to date, only Curvature thylakoid 1 (CURT1) proteins were shown to exhibit intrinsic membrane-bending capacity. Here, we show that CURT1 proteins, which play a critical role in grana margin architecture and thylakoid plasticity, also participate in de-etiolation and modulate PLB geometry and density. Lack of CURT1 proteins severely perturbs PLB organization and vesicle fusion, leading to reduced accumulation of the light-dependent enzyme protochlorophyllide oxidoreductase (LPOR) and a delay in the onset of photosynthesis. In contrast, overexpression of CURT1A induces excessive bending of PLB membranes, which upon illumination show retarded disassembly and concomitant overaccumulation of LPOR, though without affecting greening or the establishment of photosynthesis. We conclude that CURT1 proteins contribute to the maintenance of the paracrystalline PLB morphology and are necessary for efficient and organized thylakoid membrane maturation during de-etiolation.All study data are included in the article and/or SI Appendix and all raw data are available upon request from the corresponding authors.